Localization and in situ activities of homoacetogenic bacteria in the highly compartmentalized hindgut of soil-feeding higher termites (Cubitermes spp.)

Methanogenesis and homoacetogenesis occur simultaneously in the hindguts of almost all termites, but the reasons for the apparent predominance of meth anogenesis over homoacetogenesis in the hindgut of the humivorous species i s not known. We found that in gut homogenates of soil-feeding Cubitermes sp p., methanogens outcompete homoacetogens for endogenous reductant. The rate s of methanogenesis were always significantly higher than those of reductiv e acetogenesis, whereas the stimulation of acetogenesis by the addition of exogenous H-2 or formate was more pronounced than that of methanogenesis. I n a companion paper, we reported that the anterior gut regions of Cubiterme s spp, accumulated hydrogen to high partial pressures, whereas H-2 was alwa ys below the detection limit (<100 Pa) in the posterior hindgut, and that a ll hindgut compartments turned into efficient H-2 sinks when external H-2 w as provided (D. Schmitt-Wagner and A. Brune, Appl. Environ. Microbiol, 65:4 490-4496, 1999), Using a microinjection technique, we found that only the p osterior gut sections P3/4a and P4b, which harbored methanogenic activities , formed labeled acetate from (HCO3-)-C-14. Enumeration of methanogenic and homoacetogenic populations in the different gut sections confirmed the coe xistence of both metabolic groups in the same compartments. However, the in situ rates of acetogenesis were strongly hydrogen limited; in the P4b sect ion, no activity was detected unless external H-2 was added. Endogenous rat es of reductive acetogenesis in isolated guts were about 10-fold lower than the in vivo rates of methanogenesis, but were almost equal when exogenous H-2 was supplied. We conclude that the homoacetogenic populations in the po sterior hindgut are supported by either substrates other than H-2 or by a c ross-epithelial H-2 transfer from the anterior gut regions, which may creat e microniches favorable for H-2-dependent acetogenesis.